Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size

New Phytologist

Volumn 208, Issue 2, 2015, Pages 596-607

  Kelly, Laura J ^a,b   Renny Byfield, Simon ^a,c   Pellicer, Jaume ^b   Macas, Jiří ^d   Novák, Petr ^d   Neumann, Pavel ^d   Lysak, Martin A ^e   Day, Peter D ^a,b   Berger, Madeleine ^b,f,g   Fay, Michael F ^b   Nichols, Richard A ^a   Leitch, Andrew R ^a   Leitch, Ilia J ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b JODRELL LABORATORY   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d INSTITUTE OF PLANT MOLECULAR BIOLOGY   (Czech Republic)

^e MASARYK UNIVERSITY   (Czech Republic)

^f DURHAM UNIVERSITY   (United Kingdom)

^g ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Fritillaria; DNA deletion; Genome size evolution; Genome turnover; Liliaceae; Repetitive DNA; Transposable elements (TEs)

Indexed keywords

DNA; GENE EXPRESSION; GENOME; METABOLISM; MONOCOTYLEDON; MUTATION; POLYPLOIDY;

FRITILLARIA (ANGIOSPERM); LILIACEAE;

PLANT DNA;

FRITILLARIA; GENE DELETION; GENETICS; GENOME SIZE; MOLECULAR GENETICS; NUCLEOTIDE REPEAT; PLANT GENOME;

DNA, PLANT; FRITILLARIA; GENE DELETION; GENOME SIZE; GENOME, PLANT; MOLECULAR SEQUENCE DATA; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 84942835210     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13471     Document Type: Article

References (74)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
2. Ambrožová K, Mandáková T, Bureš P, Neumann P, Leitch IJ, Koblížková A, Macas J, Lysak MA. 2011. Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Annals of Botany 107: 255-268.
3. Becher H, Ma L, Kelly LJ, Kovarik A, Leitch IJ, Leitch AR. 2014. Endogenous pararetrovirus sequences associated with 24 nt small RNAs at the centromeres of Fritillaria imperialis L. (Liliaceae), a species with a giant genome. Plant Journal 80: 823-833.
4. Bennett MD, Leitch IJ. 2012. Plant DNA C-values database (release 6.0, Dec. 2012). [WWW document] URL http://data.kew.org/cvalues/. [accessed 14 October 2014].
5. Bennett MD, Leitch IJ, Price HJ, Johnston JS. 2003. Comparisons with Caenorhabditis (~100Mb) and Drosophila (~175Mb) using flow cytometry show genome size in Arabidopsis to be ~157Mb and thus ~25% larger than the Arabidopsis Genome Initiative estimate of ~125Mb. Annals of Botany 91: 547-557.
6. Bennetzen JL, Wang H. 2014. The contributions of transposable elements to the structure, function and evolution of plant genomes. Annual Review of Plant Biology 65: 505-530.
7. Bensasson D, Petrov DA, Zhang D, Hartl DL, Hewitt GM. 2001. Genomic gigantism: DNA loss is slow in mountain grasshoppers. Molecular Biology and Evolution 18: 246-253.
8. Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research 27: 573-580.
9. Blass E, Bell M, Boissinot S. 2012. Accumulation and rapid decay of non-LTR retrotransposons in the genome of the three-spine stickleback. Genome Biology and Evolution 4: 687-702.
10. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
11. D'Hont A, Denoeud F, Aury J-M, Baurens F-C, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M etal. 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488: 213-217.
12. Day PD, Berger M, Hill L, Fay MF, Leitch AR, Leitch IJ, Kelly LJ. 2014. Evolutionary relationships in the medicinally important genus Fritillaria L. (Liliaceae). Molecular Phylogenetics and Evolution 80: 11-19.
13. Doležel J, Greilhuber J, Lucretti S, Meister A, Lysak MA, Nardi L, Obermayer R. 1998. Plant genome size estimation by flow cytometry: inter-laboratory comparison. Annals of Botany 82: 17-26.
14. Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11-15.
15. Elbaidouri M, Panaud O. 2013. Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biology and Evolution 5: 954-965.
16. Elsik CG, Williams CG. 2000. Retroelements contribute to the excess low-copy number DNA in pine. Molecular and General Genetics 264: 47-55.
17. Fedoroff NV. 2012. Transposable elements, epigenetics, and genome evolution. Science 338: 758-767.
18. Givnish TJ, Ames M, McNeal JR, McKain MR, Steele PR, dePamphilis CW, Graham SW, Pires JC, Stevenson DW, Zomlefer WB etal. 2010. Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Annals of the Missouri Botanical Garden 97: 584-616.
19. Gomez-Alvarez V, Teal TK, Schmidt TM. 2009. Systematic artifacts in metagenomes from complex microbial communities. ISME Journal 3: 1314-1317.
20. Greilhuber J, Borsch T, Müller K, Worberg A, Porembski S, Barthlott W. 2006. Smallest angiosperm genomes found in Lentibulariaceae with chromosomes of bacterial size. Plant Biology 8: 770-777.
21. Greilhuber J, Doležel J, Lysak MA, Bennett MD. 2005. The origin, evolution and proposed stabilization of the terms 'Genome Size' and 'C-Value' to describe nuclear DNA contents. Annals of Botany 95: 91-98.
22. Grover CE, Wendel JF. 2010. Recent insights into mechanisms of genome size change in plants. Journal of Botany 2010: article ID 382732.
23. Hawkins JS, Kim HR, Nason JD, Wing RA, Wendel JF. 2006. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Research 16: 1252-1261.
24. Hawkins JS, Proulx SR, Rapp RA, Wendel JF. 2009. Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proceedings of the National Academy of Sciences, USA 106: 17811-17816.
25. Henderson IR. 2012. Control of meiotic recombination frequency in plant genomes. Current Opinion in Plant Biology 15: 556-561.
26. Hollister JD, Smith LM, Guo Y-L, Ott F, Weigel D, Gaut BS. 2011. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proceedings of the National Academy of Sciences, USA 108: 2322-2327.
27. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H etal. 2011. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Genetics 43: 476-481.
28. International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. Nature 436: 793-800.
29. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS etal. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
30. Kelly LJ, Leitch AR, Clarkson JJ, Knapp S, Chase MW. 2013. Reconstructing the complex evolutionary origin of wild allotetraploid tobaccos (Nicotiana section Suaveolentes). Evolution 67: 80-94.
31. Kelly LJ, Leitch AR, Fay MF, Renny-Byfield S, Pellicer J, Macas J, Leitch IJ. 2012. Why size really matters when sequencing plant genomes. Plant Ecology & Diversity 5: 415-425.
32. Kelly LJ, Leitch IJ. 2011. Exploring giant plant genomes with next-generation sequencing technology. Chromosome Research 19: 939-953.
33. Kovach A, Wegrzyn JL, Parra G, Holt C, Bruening GE, Loopstra CA, Hartigan J, Yandell M, Langley CH, Korf I etal. 2010. The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Genomics 11: 420.
34. Leitch IJ, Beaulieu JM, Cheung K, Hanson L, Lysak MA, Fay MF. 2007. Punctuated genome size evolution in Liliaceae. Journal of Evolutionary Biology 20: 2296-2308.
35. Leushkin EV, Sutormin RA, Nabieva ER, Penin AA, Kondrashov AS, Logacheva MD. 2013. The miniature genome of a carnivorous plant Genlisea aurea contains a low number of genes and short non-coding sequences. BMC Genomics 14: 476.
36. Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ. 2009. The dynamic ups and downs of genome size evolution in Brassicaceae. Molecular Biology and Evolution 26: 85-98.
37. Ma J, Devos KM, Bennetzen JL. 2004. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Research 14: 860-869.
38. Maddison DR, Maddison WP. 2002. MacClade 4: analysis of phylogeny and character evolution, Version 4.04. Sunderland, MA, USA: Sinauer Associates.
39. Metcalfe CJ, Casane D. 2013. Accommodating the load: the transposable element content of very large genomes. Mobile Genetic Elements 3: e24775.
40. Metcalf CJ, Filée J, Germon I, Joss J, Casane D. 2012. Evolution of the Australian lungfish (Neoceratodus forsteri) genome: a major role for CR1 and L2 LINE elements. Molecular Biology and Evolution 29: 3529-3539.
41. Nam K, Ellegren H. 2012. Recombination drives vertebrate genome contraction. PLoS Genetics 8: 1002680.
42. Neumann P, Koblížková A, Navrátilová A, Macas J. 2006. Significant expansion of Vicia pannonica genome size mediated by amplification of a single type of giant retroelement. Genetics 173: 1047-1056.
43. Niu B, Fu L, Sun S, Li W. 2010. Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinformatics 11: 187.
44. Novák P, Neumann P, Macas J. 2010. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11: 378.
45. Novák P, Neumann P, Pech J, Steinhaisl J, Macas J. 2013. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29: 792-793.
46. Nylander JAA. 2004. MrModeltest v2. Uppsala, Finland: Evolutionary Biology Centre, Uppsala University.
47. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A etal. 2013. The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579-584.
48. Pagel M. 1997. Inferring evolutionary processes from phylogenies. Zoologica Scripta 26: 331-348.
49. Pagel M. 1999. Inferring the historical patterns of biological evolution. Nature 401: 877-884.
50. Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker KC, Shu S, Udall J etal. 2012. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492: 423-427.
51. Pellicer J, Kelly LJ, Leitch IJ, Zomlefer WB, Fay MF. 2014. A universe of dwarfs and giants: genome size and chromosome evolution in the monocot family Melanthiaceae. New Phytologist 201: 1484-1497.
52. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA etal. 2006. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Research 16: 1262-1269.
53. R Core Team. 2014. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
54. Rambaut A, Drummond AJ. 2009. Tracer v1.5. [WWW document] URL http://tree.bio.ed.ac.uk/software/tracer. [accessed 14 October 2014].
55. Rix EM. 2001. Fritillaria: a revised classification. Oxford, UK: The Fritillaria Group of the Alpine Garden Society.
56. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MRBAYES 3.2: efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology 61: 539-542.
57. Rønsted N, Law S, Thornton H, Fay MF, Chase MW. 2005. Molecular phylogenetic evidence for the monophyly of Fritillaria and Lilium (Liliaceae; Liliales) and the infrageneric classification of Fritillaria. Molecular Phylogenetics and Evolution 35: 509-527.
58. Simillion C, Vandepoele K, Van Montagu MCE, Zabeau M, Van de Peer Y. 2002. The hidden duplication past of Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 99: 13627-13632.
59. Sun C, López Arriaza JR, Mueller RL. 2012a. Slow DNA loss in the gigantic genomes of salamanders. Genome Biology and Evolution 4: 1340-1348.
60. Sun C, Shepard DB, Chong RA, López Arriaza JR, Hall K, Castoe TA, Feschotte C, Pollock DD, Mueller RL. 2012b. LTR retrotransposons contribute to genomic gigantism in Plethodontid salamanders. Genome Biology and Evolution 4: 168-183.
61. Swofford DL. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4. Sunderland, MA, USA: Sinauer Associates.
62. The Brassica rapa Genome Sequencing Project Consortium. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43: 1035-1039.
63. The International Brachypodium Initiative. 2010. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 493: 763-768.
64. Thompson W. 1978. Perspectives on the evolution of plant DNA. Carnegie Institute of Washington Year Book 77: 310-316.
65. Van't Hof J. 1965. Relationships between mitotic cycle duration S period duration and average rate of DNA synthesis in root meristem cells of several plants. Experimental Cell Research 39: 48-58.
66. Vanneste K, Baele G, Maere S, Van de Peer Y. 2014. Analysis of 41 plant genomes supports a wave of successful genome duplications in associationwith the Cretaceous-Paleogene boundary. Genome Research 24: 1334-1347.
67. Vitte C, Bennetzen JL. 2006. Analysis of retrotransposon structural diversityuncovers properties and propensities in angiosperm genome evolution. Proceedings of the National Academy of Sciences, USA 103: 17638-17643.
68. Wang H, Liu J-S. 2008. LTR retrotransposon landscape in Medicago truncatula: more rapid removal than in rice. BMC Genomics 9: 382.
69. Wegrzyn JL, Liechty JD, Stevens KA, Wu L-S, Loopstra CA, Vasquez-Gross HA, Dougherty WM, Lin BY, Zieve JJ, Martínez-García PJ etal. 2014. Unique features of the loblolly pine (Pinus taeda L.) megagenome revealed through sequence annotation. Genetics 196: 891-909.
70. Wenzel W, Hemleben V. 1982. A comparative study of genomes in angiosperms. Plant Systematics and Evolution 139: 209-227.
71. Whitelaw CA, Barbazuk WB, Pertea G, Chan AP, Cheung F, Lee Y, Zheng L, van Heeringen S, Karamycheva S, Bennetzen JL etal. 2003. Enrichment of gene-coding sequences in maize by genome filtration. Science 302: 2118-2120.
72. Wicker T, Keller B. 2007. Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Research 17: 1072-1081.
73. Wicker T, Taudien S, Houben A, Keller B, Graner A, Platzer M, Stein N. 2009. A whole-genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. Plant Journal 59: 712-722.
74. Zonneveld B. 2010. New record holders for maximum genome size in eudicots and monocots. Journal of Botany 2010: article ID 527357.